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Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice

BACKGROUND: The mammalian gut microbiota influences a wide array of phenotypes which are relevant to fitness, yet knowledge about the transmission routes by which gut microbes colonise hosts in natural populations remains limited. Here, we use an intensively studied wild population of wood mice (Apo...

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Autores principales: Wanelik, Klara M., Raulo, Aura, Troitsky, Tanya, Husby, Arild, Knowles, Sarah C. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10230743/
https://www.ncbi.nlm.nih.gov/pubmed/37259168
http://dx.doi.org/10.1186/s42523-023-00247-7
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author Wanelik, Klara M.
Raulo, Aura
Troitsky, Tanya
Husby, Arild
Knowles, Sarah C. L.
author_facet Wanelik, Klara M.
Raulo, Aura
Troitsky, Tanya
Husby, Arild
Knowles, Sarah C. L.
author_sort Wanelik, Klara M.
collection PubMed
description BACKGROUND: The mammalian gut microbiota influences a wide array of phenotypes which are relevant to fitness, yet knowledge about the transmission routes by which gut microbes colonise hosts in natural populations remains limited. Here, we use an intensively studied wild population of wood mice (Apodemus sylvaticus) to examine how vertical (maternal) and horizontal (social) transmission routes influence gut microbiota composition throughout life. RESULTS: We identify independent signals of maternal transmission (sharing of taxa between a mother and her offspring) and social transmission (sharing of taxa predicted by the social network), whose relative magnitudes shift as hosts age. In early life, gut microbiota composition is predicted by both maternal and social relationships, but by adulthood the impact of maternal transmission becomes undetectable, leaving only a signal of social transmission. By exploring which taxa drive the maternal transmission signal, we identify a candidate maternally-transmitted bacterial family in wood mice, the Muribaculaceae. CONCLUSION: Overall, our findings point to an ontogenetically shifting transmission landscape in wild mice, with a mother’s influence on microbiota composition waning as offspring age, while the relative impact of social contacts grows. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00247-7.
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spelling pubmed-102307432023-06-01 Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice Wanelik, Klara M. Raulo, Aura Troitsky, Tanya Husby, Arild Knowles, Sarah C. L. Anim Microbiome Research BACKGROUND: The mammalian gut microbiota influences a wide array of phenotypes which are relevant to fitness, yet knowledge about the transmission routes by which gut microbes colonise hosts in natural populations remains limited. Here, we use an intensively studied wild population of wood mice (Apodemus sylvaticus) to examine how vertical (maternal) and horizontal (social) transmission routes influence gut microbiota composition throughout life. RESULTS: We identify independent signals of maternal transmission (sharing of taxa between a mother and her offspring) and social transmission (sharing of taxa predicted by the social network), whose relative magnitudes shift as hosts age. In early life, gut microbiota composition is predicted by both maternal and social relationships, but by adulthood the impact of maternal transmission becomes undetectable, leaving only a signal of social transmission. By exploring which taxa drive the maternal transmission signal, we identify a candidate maternally-transmitted bacterial family in wood mice, the Muribaculaceae. CONCLUSION: Overall, our findings point to an ontogenetically shifting transmission landscape in wild mice, with a mother’s influence on microbiota composition waning as offspring age, while the relative impact of social contacts grows. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00247-7. BioMed Central 2023-05-31 /pmc/articles/PMC10230743/ /pubmed/37259168 http://dx.doi.org/10.1186/s42523-023-00247-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Wanelik, Klara M.
Raulo, Aura
Troitsky, Tanya
Husby, Arild
Knowles, Sarah C. L.
Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
title Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
title_full Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
title_fullStr Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
title_full_unstemmed Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
title_short Maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
title_sort maternal transmission gives way to social transmission during gut microbiota assembly in wild mice
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10230743/
https://www.ncbi.nlm.nih.gov/pubmed/37259168
http://dx.doi.org/10.1186/s42523-023-00247-7
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